Abstract
Global production of tomato has been hampered by the increased incidences of tomato viral disease. The high genetic heterogeneity of tomato plant viruses, because of their high mutation rates, has lead to ineffective control strategies and the fast spread of the viruses. Viruses utilize the resources in host plants for their replication. Therefore, identification and removal of the non-redundant proteins in the tomato plant based on the biological properties of the virus combined with an RNAi strategy may be a future control strategy. In this review, fourteen tomato viral diseases and their causal agents are reviewed and the control strategies for tomato viral diseases are discussed.
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Introduction
Tomato, Solanum lycopersicum L., is a major cultivated agriculture crop all around the globe, which garnered a worldwide production of over 180 million tonnes in 2017 (FAOSTAT 2019). Based on the data from FAOSTAT (2019), China has the highest tomato production with over 59 million tonnes in 2017 followed by Turkey, USA, Egypt, Italy, Spain, Mexico, Nigeria, Brazil and the Russian federation. Tomato can be consumed fresh or sold as soups, sauces and ketchup (Harvey et al. 2002). Besides being an edible food, several secondary metabolites found in tomato can be used as anti-oxidant and may also have anti-cancer functions (Raiola et al. 2014). However, as a crop, the high susceptibility of tomato to virus disease causes yield decline of between 70 and 95% and could affect supply (Rashid et al. 2016). Plant viruses consist of both DNA and RNA viruses where they can be in the form of a single- or double-stranded DNA or RNA (Wang et al. 2012). The difference between DNA and RNA viruses is their mode of replication where DNA viruses rely on the DNA replication machinery of the host and RNA viruses do not rely on the cellular DNA machinery of the host (Wang et al. 2012). Control of plant viruses remains an important agriculture issue due to its high mutation rate that promotes divergence of genetic strains (Garcia-Arenal et al. 2001). This leads to the need to study the host–virus interactions and viral gene expression to develop sustainable and efficient viral control strategies. This review targets to collate the current information on the viral genome, transmission methods, viral vectors and host plants as well as disease symptoms of virus diseases infecting tomato to provide a better understanding of each virus. Additionally, current and potential control strategies will be discussed.
Types of tomato plant viruses
Tomato DNA virus
The genomes of tomato plant viruses are either DNA or RNA (Table 1). Among all the major tomato viral diseases, only viruses from the family Geminiviridae are DNA viruses. In this family, the genus begomovirus plays a crucial role as a pathogen that causes serious impact on economically important crops globally (Zubair et al. 2017). Geminiviruses are ranked second for the number of viruses in its family that affects both monocot and dicot plants (Rojas 2004). However, according to Cantu-Iris et al. (2019), begomoviruses infect dicot plants solely. According to Zhou (2013), begomovirus affects a wide range of dicot host species including Carica papaya, Capsicum annuum and another 40 hosts that are listed in his review. Begomoviruses which replicate in the nucleus of the host have a twinned capsid morphology, with either a monopartite or bipartite circular single-stranded DNA (ssDNA) (Hosseini et al. 2010). Satellite DNAs such as alpha satellites and beta satellites (Fig. 1) can be associated with the monopartite begomoviruses (Zhou 2013). There are also delta satellites which are non-coding satellites associated with the begomovirus (Hassan et al. 2016). According to Rojas et al. (2005), these viruses replicate through double-stranded DNA (dsDNA) by a rolling circle replication (RCR) mechanism. First, a dsDNA intermediate will be formed from the ssDNA genome and the viral ssDNA begins to amplify through the starting position of RCR which is found within the conserved sequence TAATATTAC. Finally, the newly formed ssDNA will be encapsidated and then moved to the adjacent cells (Gutierrez 2002). Among begomoviruses, the Tomato yellow leaf curl (TYLC) has the most significant impact over tomato production by causing disease in subtropical and tropical regions worldwide (Moriones et al. 2011). A review of the “top 10 plant virus list” by Scholthof et al. (2011) showed that TYLC ranked third based on its scientific and economic importance while Suresh et al. (2017) listed a total of 96 other species of begomovirus across the world that are infecting tomato.
There are six proteins (two ORFs in the virion sense and four ORFs in the complementary sense in DNA A; Fig. 1) encoded by monopartite begomoviruses, which are the genes that encode for the coat protein (V1), pre-coat protein (V2), replication-associated protein (C1), transcriptional activator protein (C2), the replication enhancer protein (C3) and the protein involved in movement and symptom development (C4, Ammara et al. 2015). V1 and V2 are in virion sense strand, whereas C1, C2, C3 and C4 in complementary sense strand (Srivastava et al. 2015). Each protein holds a different function; for instance, the coat and pre-coat protein is responsible for virus movement in the plant, but the coat protein is also responsible for the movement between plants through insect vectors (Diaz-Pendon et al. 2019). While C1 and C3 ORFs are involved in replication, C2 is involved in transactivation expression of the virion sense genes and C4 determines (or is related to) pathogenicity (Zerbini et al. 2017).
Beet curly top virus (BCTV; Table 1; Fig. 1) is the causal agent of the curtovirus disease from the family Geminiviridae that is classified in the genus curtovirus (Jeger et al. 2017). This species was first discovered infecting sugar beet in 1967 in Iran (Gibson 1967). The susceptible hosts comprise of cucurbit, bean, pepper, beet, tomato, potato and weed species (Lam et al. 2009). These viruses have circular ssDNA genome and encapsidated within twinned icosahedral particles (Lam et al. 2009). The genome of this genus possesses one intergenic region (IR), three virion sense and four complementary sense ORFs (Varma and Malathis 2003; Fig. 1). The complementary sense gene products are replication and transcription regulator proteins such as C2, C4, replication protein (Rep) and replication enhancer proteins (REn/C3) (Bolok Yazdi et al. 2008). Three other proteins are coded by the virion sense strand, including a V2 protein, movement protein (MP) and coat protein (CP) (Gutierrez 2002; Hosseini et al. 2010).
Tomato RNA virus
Tomato Monopartite RNA virus
The RNA viruses that affect tomato are all single-stranded viruses, but the genomes are either monopartite, bipartite or tripartite. Potexvirus (family: Alphaflexiviridae; King et al. 2012), Tobamovirus (family: Virgaviridae; King et al. 2012), Potyvirus (family: Potyviridae; Gibbs and Ohshima 2010) and Tombusvirus (family: Tombusviradae; Nasir et al. 2016) are made up of monopartite positive single-stranded RNA (ssRNA) genome (Table 1; Chung et al. 2008; Jeger et al. 2017; Luria et al. 2017; Verchot-Lubicz et al. 2007). Pepino mosaic virus (PepMV; Fig. 2) from genus Potexvirus is a flexuous, rod-shaped particle (Hanssen et al. 2010). The Potexvirus spp. consists of a ssRNA of positive polarity and contains five ORFs (Verchot-Lubicz et al. 2007; Fig. 2). The ORFs include replicase gene, triple gene block (TGB) encoding TGB1, TGB2 and TB3 for viral movement and suppress silencing and lastly coat protein (Agirrezabalaet al. 2015). According to Moreno-Perez et al. (2014), molecular and biological characteristics of PepMV categorize it into six strains, including the North American strain (US1/CH1), the recombinant strain (US2), European strain (EU), Chilean strain (CH2), the original Peruvian strain (LP) and the new Peruvian strain (PES). PepMV was found to infect solanaceous crops as well as test plants such as S. tuberosum, S. melongena, Physalis florida, Nicotiana benthamiana and Datura stramoniu, with most of the host species in the Solanaceae family (Blystad et al. 2015).
For the tobamoviruses genus, viruses that have been found in tomato are Tobacco mosaic virus (TMV), Tomato mottle mosaic virus (ToMMV; Table 1; Fig. 2), Tomato mosaic virus (ToMV), Tobacco mild green mosaic virus (TMGMV) and Tomato brown rugose fruit virus (ToBRFV) (Dombrovsky and Smith 2017). TMV, TMGMV and ToMV affect tomato production worldwide (Suresh et al. 2017). Tobamoviruses have rod-shaped particles (Luria et al. 2017). The susceptible crops of the tobamovirus include the Cucurbitaceae and Solanaceae families (Dombrovsky and Smith 2017). Their genome possesses four ORFs (Li et al. 2017). The first two ORFs encode the replication protein while ORF-3 and ORF-4 encode MP and CP, respectively (Ishibashi and Ishikawa 2016; Fig. 2).
Species of Potyvirus genus include Potato virus Y (PVY) and Tobacco etch virus (TEV) (Table 1; Fig. 2). The genome of potyviruses consists of a short ORF placed in the long ORF (Chung et al. 2008). Potyviruses have a positive-sense RNA genome with flexuous filament particles (Kenyon et al. 2014). This RNA can perform as a messenger RNA (mRNA) where the 5′ non-coding part can be used as a promoter for translation (Sharma et al. 2014). The long ORF in the genome will be translated into a polyprotein and further cut into 10 useful proteins by virus-encoded proteinase (Trigiano et al. 2003; Fig. 2) including the CP, nuclear inclusion b protein (Nib), nuclear inclusion a protein (NIa-Pro), nuclear inclusion a linked VPg protein (NIa-VPg), 6K2 protein, C1 protein, 6K1 protein, P3 protein, helper component protein (HC-Pro) and P1 protein (Trigiano et al. 2003). The most distinctive characteristics of the potyviruses are the formation of the inclusion bodies in the affected cells (Edwardson 1974). Based on the supplementary data of Gibbs and Ohshima (2010), host plants of PVY are not only tomato but Capsicum and Solanaceous species as well. Tsedaley (2015) has also compiled the natural and experimental host range of PVY in his review which includes Capsicum and Solanaceous species as well as ornamental plants and weeds.
Similar to Potyvirus, Tomato bushy stunt virus (TBSV; Table 1; Fig. 2) which is a part of Tombusvirus genus has a tiny unenclosed virus with isometric particles of diameter approximately 30 nm (Nawazet al. 2014). This monopartite positive-sense ssRNA virus possesses five ORFs in its genome (Nawazet al. 2014; Fig. 2). Proteins coded by the first and second ORF are needed for replication of the virus (Scholthof et al. 1995). ORF-3 coded for coat protein, while the viral movement protein codes for cell-to-cell movement of the virus and in some plants for symptom determination is encoded by ORF-4 (Scholthof et al. 1993). ORF-5 plays a part in causing the necrotic symptoms as well as virus long-distance transmission (Hafez et al. 2010). TBSV affected areas are Tunisia, USA, Portugal, Morocco, Germany, Canada, France, Italy, Great Britain, Spain and Argentina (Suresh et al. 2017). The hosts of this virus are lettuce, spinach, apple, pear, tobacco, tomato, eggplant, tulip and pepper (Artelli et al. 2001).
Tomato bipartite RNA virus
The genus Crinivirus belongs to the family of Closteroviridae and consists of positive-sense bipartite ssRNA genome (Wintermantel 2004). The member of this family all consists long and flexuous rod-shaped virions (Kiss et al. 2013). The first RNA encodes four ORFs for replication-associated proteins (ORF1a, ORF1b, ORF2 and P5; Fig. 3). RNA-2 on the other hand codes for putative MP, CP, CPm (minor coat protein) and HSP70 homolog (Wintermantel et al. 2005). According to Wisler et al. (1998), this tomato virus was first assigned to the genus Closterovirus, but later it was attributed to the genus Crinivirus (Fauquet and Mayo 1999). Members of this genus are Tomato chlorosis virus (ToCV; Table 1; Fig. 3) and Tomato infectious chlorosis virus (TICV) (Hanssen et al. 2010). ToCV was named after TICV from the differences in RNA sequence, vector specificity and host range. Other than L. esculentum (tomato), hosts of ToCV include Zinnia elegans (zinnia, Tsai et al. 2004), C. annuum (sweet pepper; Lozano et al. 2004) and S. tuberosum (potato; Lee et al. 2018). Infected areas of TICV are North America, Europe, Turnisia, Asia and Middle East, whereas ToCV has been found across the globe (Suresh et al. 2017).
Torradovirus genus is a bipartite virus with a positive ssRNA genome encapsidated into nonenveloped icosahedral particles, consisting of three open reading frames (ORF), RNA-1 encodes one ORF and RNA-2 encodes two ORFs (Sanfacon et al. 2009; Verbeek et al. 2013). The ORF in RNA-1 codes for the protease cofactor (Pro-Co), helicase (Hel), protease (Pro) and RNA-dependent RNA polymerase (RdRp) (NC_009013.1). Two ORFs in RNA-2 include ORF1 encoding a polyprotein which includes the movement protein (MP), coat protein Vp35, Vp26 and Vp23 (Fig. 3; NC_009032.1). These viruses were placed in the new family Secoviridae that comprises all plant viruses in the order Picornavirales and comprises of genus such as Torradovirus (Sanfacon et al. 2009). There are three new species belonging to the Torradovirus novel genus, which are Tomato marchitez virus (ToMarV), Tomato torrado virus (ToTV; Table 1; Fig. 3) and tomato apex necrosis virus (ToANV; Verbeek et al. 2008). The discovery of these viruses was in 2001 where symptoms such as necrotic or burn-like were seen in tomato crops in the southeast of Spain (Alfaro-Fernandez et al. 2007). The early diagnosis initially showed the presence of PepMV, but after further studies, it showed different symptoms and ToTV was proposed (Verbeek et al. 2007). After 2003, the same disease symptoms were seen in Mexican tomato crops where the tomato spotted wilt virus (TSWV) was first suspected to be the causal agent of this disease (Turina et al. 2007). However, the presence of the isometric viral particles as well as the characterization and the partial sequencing showed differences; thus, the ToANV was proposed (Turina et al. 2007). Even though it is highly similar to ToTV, the subsequent nucleotide sequence of the three ORFs was distinctive and so the virus ToMarV was suggested (Verbeek et al. 2008). The hosts of the ToTV were experimentally tested by Amari et al. (2008) and showed that this virus systematically infects S. melongena, S. lycopersicum, C. annuum, Physalis floridana, N. tabacum, N. rustica, N. glutinosa and N. benthamiana.
Tomato Tripartite RNA virus
Among the five genera with tripartite genomes, four out of five are from the family Bromoviridae, for instance, Cucumovirus, Alfamovirus, Anulavirus and Ilarvirus. Viruses from Cucumovirus and Alfamovirus have icosahedral capsids (Al-Saleh and Amer 2013; Krenz et al. 2015), whereas Anulavirus and Ilarvirus have quasi-spherical particles (Bratsch et al. 2019; Lapidot et al. 2010).
Alfalfa mosaic virus (AMV; Table 1; Fig. 4) is a member of the genus Alfamovirus and in the family Bromoviridae which possesses three plus-sense polarity single-stranded RNA (ssRNA) molecules (Al-Abrahim 2014; Fig. 4). The RNA is classified as RNA 1 to RNA 3 in descending order of molecular size, and each is enclosed into B, M and Tb components (Abdalla et al. 2015). AMV also affected some other vegetable crops such as eggplant (S. melongena L.), lettuce (Lactuca sativa L.), pea (Pisum sativum L.), bean (Phaseolus vulgaris L.), celery (Apium graveolens L.), pepper (C. annuum L.), alfalfa (Medicago sativa L.), borage (Borago officinalis L.), tuberous comfrey (Symphytum tuberosum L.), cowpea (Vigna unquiculata (L.) Walp), mung bean (V. mungo (L.) Hepper), chickpea (Cicer arietinum L.) and tumble pigweed (Amaranthus albus L.) (Malor et al. 2002; Bellardi and Benni 2005; Zitikaite and Samuitiene 2008; Fidan et al. 2012; Al-albrahim 2014).
For the Cucumber mosaic virus (CMV; Table 1; Fig. 4) that belongs to the genus Cucumovirus, it encodes five proteins (Palukaitis and Garcia-Arenal 2003). RNA 1 and 2 are for viral replication and encode the 1a and 2a proteins, respectively (Pumplin and Voinnet 2013), while RNA 4A (subgeneomic RNA from RNA 2) encodes 2b protein that suppresses RNA silencing (Wang et al. 2012). RNA 3 that is translated from subgenomic RNA 4 encodes the movement protein (MP) and the coat protein (CP) (Jacquemond 2012). There are three subgroups of CMV strains (IA, II and IB) that have been categorized in which IA and II have spread globally, whereas IB is focused in Asia (Hasiów-Jaroszewska et al. 2018). According to Geetanjali et al. (2011), CMV causes damage to species under family Solanaceae and Cucurbitaceae, whereas Mochizuki and Ohki (2012) stated that CMV also caused diseases in the families Leguminosae, Brassicaceae, Gramineae other than Solanaceae and Cucurbitaceae.
Pelargonium zonate spot virus (PZSV; Table 1; Fig. 4) is the type member of the genus Anulavirus (Gioliti et al. 2014). The genome is made up of three linear positive-sense ssRNAs (RNA-1, RNA-2 and RNAp-3; Fig. 4) that encode four proteins (Codoner and Elena 2006). RNA-1 encodes protein 1a, RNA-2 encodes protein 2a which consists of RNA-dependent RNA polymerase (RdRP), and RNA-3 encodes movement and coat protein (Finetti-Sialer and Gallitelli 2003). PZSV was first identified from Pelargonium zonale (Quacquarelli and Gallitelli 1979). Later, it was reported as causal agent of tomato diseases in Southern Italy by Gallitelli (1982) followed by identification in tomato in other countries. The distribution includes Spain, USA, Israel, Italy and France (Suresh et al. 2017). The hosts of this virus include plants from the Solanaceae, Actinidiaceae, Brassicaceae and Asteraceae (Li et al., 2014).
Ilarviruses (family Bromoviridae) have a genome consisting of three positive ssRNAs enclosed in quasi-spherical particles (Bratsch et al. 2019; Fig. 4). RNA-1 codes for replicase protein, and RNA-2 and RNA-3 encode replicase protein, RNA-dependent RNA polymerase, MP and CP proteins, respectively (Pallas et al. 2013). Additional tomato disease causal agents from the ilarvirus are Tobacco streak virus (TSV; Table 1; Fig. 4) discovered in USA in 1982 where the report showed global distribution (Zitter 2014). Other examples are tomato necrotic spot virus (ToNSV) and Tomato necrotic streak virus (TomNSV) which were discovered in California and Florida, respectively (Badillo-Vargas et al. 2016;; Batuman et al. 2009). PMoV also infects plants such as Mirabilis jalapa and Capsicum annuum (Janssen et al. 2005; Parrella 2002). The expanding host range of this virus is due to the ability of it to transmit with sap extracts through physical inoculation (Aparicio et al. 2018). Thus, it can transmitted to different families such as Solanaceae, Cucurbitaceae, Fabaceae, Brassicaceae, Chenopodiaceae Aizoaceae, Lamiaceae, Asteraceae, Malvaceae, Portulacaceae and Ranunculaceae as compiled by Aparicio et al. (2018) in their review.
According to Abudurexiti et al. (2019), Orthotospovirus spp. (family Tospoviridae) which includes type virus tomato spotted wilt virus (TSWV; Table 1; Fig. 4), and capsicum chlorosis virus (CaCV), groundnut ringspot virus (GRSV), tomato chlorotic spot virus (TCSV) are classified based on the International Committee of Taxonomy of Viruses (ICTV) (Fig. 5). Other than these, the EFSA Panel on Plant Health (PLH 2012) also listed other orthotospoviruses that have infected tomato naturally and experimentally, for instance, tomato yellow ring virus (TYRV), groundnut bud necrosis virus (GBNV), tomato necrotic ringspot virus (TNRV), tomato necrotic spot virus (TNSV), tomato zonate spot virus (TZSV), alstroemeria necrotic streak virus (ANSV), chrysanthenum stem necrosis virus (CSNV), polygonum ringspot virus (PolRSV), watermelon bud necrosis virus (WBNV) and watermelon silver mottle virus (WSMoV).
TSWV is generally spherical in shape and consists of three ssRNA genomes such as small (S), medium (M) and large (L) that share the genomic features of orthotospoviruses (Turina et al. 2016; Gupta et al. 2018). The RNA-dependent RNA polymerase that is involved in RNA replication is coded by negative L RNA (Kim et al. 2013), while M RNA codes a guide for GN/GC glycoprotein (Whitfield et al. 2008). S RNA encodes nucleocapsid protein (Gupta et al. 2018). Furthermore, there are other proteins such as non-structural protein (NS) in the viral sense of M RNA and non-structural protein (NSs) in the viral sense of sRNA through an ambisense coding strategy (Guo et al. 2017). According to Gupta et al. (2018), one of the most detrimental viruses among the orthotospoviruses is TSWV with a host range of more than 85 families. The success of the TSWV infection in the host is achieved through the highly coordinated expression of these proteins within the hosts of tospoviruses that include tobacco, potato, pepper, groundnut, lettuce and bean other than tomato (Gupta et al. 2018).
Vector and transmission methods of plant viruses in commercial cropping system
Most plant viruses rely on insect vectors to spread to the next host (Gadhave et al. 2019). So control measures can be developed by studying the transmission vector of the viruses in order to increase the understanding of their epidemiology. Plant viruses that are spread persistently have a strong relationship with their insect vectors (Gadhave et al. 2019). Bermisia tabaci is the vector for both DNA and RNA viruses infecting Begomovirus spp., Crinivirus spp. and Torradovirus spp. Jiao et al. (2013) reported that B. tabaci is a natural vector that transmits viruses in a persistent and circulative manner. Chiemsombat et al. (2018) reaffirmed that begomoviruses are spread through whiteflies B. tabaci in a persistent manner. In addition to B. tabaci, both Crinivirus spp. and Torradovirus spp. can also be transmited by Trialeurodes whiteflies as their vector (Verbeek et al. 2013; Wintermantel 2004). TICV is disseminated by T. vaporariorum, and ToCV is disseminated by whitefly T. abutilonea and also B. tabaci (Middle East-Asia Minor 1 (MEAM1), Mediterranean (MED) and New World Group; Navas-Castillo et al. 2000; Wintermantal and Wisler 2006; de Moraes et al. 2018). Torradovirus spp. are transmitted by T. Trialeurodes and B. tabaci in a semi-persistent and stylet-borne manner (Verbeek et al. 2013).
For the transmission by aphids in Cucumovirus, Alfamovirus and Potyvirus, the transmissions of potyviruses are either through aphids, seed or contaminated living plant materials (Gibbs and Ohshima 2010). Tsedaley (2015) has also reported that PVY can be spread through mechanical means or through wounds of infected plant sap. PVY is transmitted by aphid in a non-persistent manner (Gadhave et al. 2019). A compilation has been published by Sigvald (1985) and Tsedaley (2015) on the few aphid species that have transmitted PVY, for instance, Myzus persicae, Rhopalosiphum padi, Acryrthosiphon pisum, Metopolophium dirhodum, Cavariella aegopodi, Aphis species and others.
According to Zitikaite and Samuitiene (2008), AMV is spread to the surrounding crops via at least 15 aphid species either in a stylet-borne or in a non-persistent manner. Other than that, the AMV can also be transmitted by mechanical or grafting methods (Fidan et al. 2012). In addition, CMV can also be either spread mechanically through plant saps, seeds or by aphids in a non-persistent manner (Palukaitis and Garcia-Arenal 2003). Aphids that have transmitted the CMV have been reported by Palukaitis et al. (1992) in his review where the A.gossypii and M. persicae are the most commonly associated with CMV transmission.
Other than whiteflies and aphids as vectors, thrips are also the vector for some tomato viruses. Anulavirus, Ilarvirus and orthotospovirus are transmitted by thrips species (Gilbertson et al. 2015; Gupta et al. 2018; Vovlas et al. 1989). According to Vovlas et al. (1989), transmission of PZSV is through seed of Diplotaxis erucoides and not through tomato seed. Preliminary study also showed that thrips species carry the pollen grain of D. erucoides on its body in an unusual manner and transfers the virus while they feed on the flowers of tomato (Vovlas et al. 1989). Transmissions of the ilarviruses are through either seed or thrips-mediated pollen (Gilbertson et al. 2015). Orthotospoviruses can be disseminated and replicated in their thrips, tiny insects vectors, such as Frankliniella occidentalis (Gupta et al. 2018).
Although Potexvirus mainly spread from plant to plant without a vector (King et al. 2012), evidences have shown that bumblebees; fungus; and whitefly can act as the vector for PepMV (Alfaro-Fernándezet al. 2009; Noëlet al. 2014; Shipp et al. 2008). Potexvirus spp. can be transmitted mechanically as well (Hanssen et al. 2010). The transmission method of Tombusvirus is not through an insect vector but through mechanical methods, propagation material or seed and pollen (Hafez et al. 2010). Same goes to Tobamovirus, even though there is no vector for virus transmission, they can spread mechanically through farming process by persisting long time in contaminated soil (Candemir et al. 2012). These viruses are very stable and remain infectious for many years (Dombrovsky and Smith 2017). In damaged roots, these viruses will infect the plants (Almeida et al. 2018). In addition, they can also spread through infected seed coat which further infects the damaged roots during transplantation (Liu et al. 2014). Tobamoviruses are the seed-borne viruses (Luria et al., 2017). Moreover, these viruses can also be spreading through greenhouse design, equipments, workers’ hands and ropes as well as the transportation in field (Reingold et al. 2016).
Beet leafhopper is a vector for Curtovirus spp. According to Jeger et al. (2017), BCTV is only transmitted through beet leafhoppers such as Circular tenellus. This insect can transport the virus for around 30 days but without involving virus replication (Soto and Gilbertson 2003). The Curtovirus spread by C. tenellus is in a circulative and non-propagative manner (Nusayr and Creamer 2017).
Disease spectrum of tomato viruses
The disease spectrum caused by different viruses infecting tomato as listed above consists of a wide range of symptoms and pathology. TMV the type species of tobamoviruses in family Virgaviridae (King et al. 2012; Scholthof et al. 2011) causes mild to severe mosaic symptoms in tomato and was also the first ever plant virus described (Mayer 1886). The viruses from the Tobamovirus genus not only spread globally but also adapt to different environments and cause a range of symptoms (Almeida et al. 2018). Symptoms on tomato caused by the tobamovirus ToMV include curling and deformation of leaves with inner browning, mosaic and irregular ripening (Fahim and Din 2017).
Pratapet al. (2008) described CMV as one of the most detrimental viruses infecting tomato. They are a species of the genus Cucumovirus whose members have a host range of more than 1200 distinct plant species within 500 genera from more than 100 families (Jacquemond 2012). Cucumber mosaic disease on tomato shows symptoms such as mosaic, necrosis, mottling, narrowing or shoes-string of leaves and stunting. Other than cucumovirus, the pepino mosaic disease caused by PepMV is a widespread pathogen that infects most of the tomato crops around the world (Hanssen and Thomma 2010). It was first described in 1980 when it infected pepino (Solanum muricatum) in Peru (Jones et al. 1980). In 1999, the PepMV was found infecting tomato crops in Europe (van der Vlugt et al. 2000). The significant fruit marbling symptoms make it an important and recognizable symptom of PepMV (Hanssen et al. 2008). Other symptoms are irregular or blotchy ripening of the tomato fruit, distorted young leaves, yellow angular spots on the leaves, leaf scorching, leaf mosaics and leaf blistering (Hanssen et al. 2009).
Tomato bushy stunt disease is caused by TBSV and was discovered by Smith in England in 1935 (Smith 1935). According to Martelliet al. (1988), TBSV is a soil-borne virus that can be maintained in soil, and therefore, the plant is infected in the roots locally. The infected plants will show symptoms on the fruit such as rings and lines as well as a reduction in size (Gerik et al. 1990). Other than that, distortion of leaves and fruit, necrosis, slow and thick growth pattern, chlorotic spot and wrinkling of leaf can be observed as well (Luis-Arteaga et al. 1996).
PVY potyvirus disease was placed in the top five most important viruses causing global loss in tomato plants by Scholthof et al. (2011). The genus Potyvirus from the family Potyviridae found worldwide and infect both monocot and dicot plants (Gibbs and Ohshima 2010) and was first described in the 1920s by Kenneth Smith in the UK (Smith 1931). Another species of Potyvirus, TEV, was discovered by Valleau and Johnson (1928) in Kentucky. Symptoms such as necrosis, mottling on leaf, wrinkle and leaf distortion can be seen on potyvirus TEV-infected tomato plants. In addition, symptoms such as fruit mottling are also observed (Zitter 1991). For the crinivirus infections, yellow interveinal and thick mature leaves are some of the symptoms seen. Fruits may show no specific symptom, although they can be smaller, lesser and earlier in ripening (Dalmon et al. 2009).
Based on Panagopoulos (2000), tomato double-streak disease is caused by the mixed infection of two types of virus which are the PVX and ToMV. Otsuki and Takebe (1976) observed that the two were able to interact and replicate in the same cell. Tomato crops grown in infected potato fields often have a high chance of being infected by PVX whose primary host is the potato crops (Cerkauskas 2005). Generally, tomato double-virus streak disease causes dwarf plant, curl leaves, long brown to dark streaks on the leafstalk, veins and the stalk; on the other hand, the uneven brown gangrene spots of different sizes will be seen in infected fruits as well as irregular ripening (Zitter and Provvideti 1984). Both viruses are economically important on their own causing severe yield losses.
For the torrado virus disease, the initial symptoms of the infection are light green or yellowing below the leaflets surrounding the necrotic spots. Later, severe necrosis will be seen in the leaves and fruit resulting in diminishing growth (Verbeek et al. 2007). Pelargonium zonate spot disease shows symptoms such as chlorotic and necrotic rings as well as line patterns on the leaves and fruit, which result in plant stunting, leaf malformation and fruit reduction, subsequently causing death (Gallitelli 1982). Parietaria mottle virus (PMoV), which causes ilarvirus disease, was first found infecting Parietaria officinalis L. in Italy (Caciagli et al. 1989). A few years later, PMoV infecting tomato was reported in Piedmont, Italy by Ramasso et al. (1997). The symptoms of PMoV can be observed in two stages, initial infection and later infection (Aparicioet al. 2018). During the early stage of the infection, symptoms such as necrosis of leaves, stem and apex can be seen, while in the later stage, plants will show necrotic mosaic symptoms on the newly emerging shoot, while corky rings and brown patches of scars will be formed on the fruit, followed by the distortion and color changes on the fruit (Aparicioet al. 2018).
For the disease caused by Orthotospovirus spp., the viruses have been found infecting tomato plants throughout Asia, Middle East and Australia (Dong et al. 2008). Despite this, Orthotospoviruses are also found in South Africa and South America (de Avila et al. 1993), USA (Webster et al. 2011) as well. The incidence of infection by Orthotospovirus spp. has risen with the increase in the population of the western flower thrips (Frankliniella occidentalis; Rojas and Gilbertson 2008). TSWV was first identified in 1915, but it was only in 1930 that it was recognized as the causal agent of this disease (Oliver and Whitfield 2016). The disease symptoms first appear in the foliage stage, where the leaflets show small and dark green chlorotic lesions, and later the chlorotic lesions will combine to and give a bronze necrotic appearance resulting in wilting necrosis spreads to the terminal shoots (Melzer et al. 2012). On the other hand, if the mature plants are infected, the distinguishable symptoms are discolored blotches or concentric rings on the fruits (Melzer et al. 2012).
Alfalfa mosaic disease caused by AMV is a global pathogen and causes infection in wide range of plant species (Loebenstein et al. 2001). According to Zitikaite and Samuitiene (2008), alfalfa seems to be the overwintering host of AMV where the infected tomatoes farm is generally near alfalfa fields. Fruits and the interveinal region of the leaves on the infected tomato plants showed bright yellow mottle symptoms, and later, the leaf will turn yellowing followed by plant stunting and leaflet distortion (Zitikaite and Samuitiene 2008).
Geminiviruses which include the Curtovirus and Begomovirus affect the photosynthetic process of infected plants by invading the phloem cells which subsequently causes starch declination and flower and fruit disruption (Rojas 2004). The symptoms of begomoviruses include retarded growth, wrinkling, twisted leaf, mottle, thick and yellow vein and small leaves (Inoue-Nagata et al. 2016), whereas symptoms of curtovirus disease include retarded plant growth, wrinkling, yellowing and swelling vein, phloem hyperlasia and twisted leaf (Hosseini 2010).
Control strategies
Basic control strategy of plant virus diseases starts with conventional good farming practices. Islam (2017) has suggested several methods to handle virus disease at the farmer stage which included crop rotation to prevent the planting of similar host, selection of healthy cuttings or seeds; removal of the disease infected plants from the farm; and removal of weeds or hosts that are potential reservoir of the virus or its vector. Additionally, the use of appropriate insecticides to eradicate the vector insects, soil fumigation, use of resistant variety and last but not least to provide education on good practices to the farmers is vital (Islam 2017). Rojas et al. (2018) reported that the use of resistant varieties was an effective strategy in controlling the tomato yellow leaf curl disease. Biswa et al. (2011) also suggested methods such as organic farming and cross-protection which have been used to control ToMV.
The rapid adaptive nature and ability to utilize resources in host plants for their replication make viruses a challenge to the crop industries. Additionally, plant viruses generally do not spread itself instead it relies on vectors such as insect, fungus, nematode or arthropod to reach their target plants (Dietzgen et al. 2016). Understanding that genome of viruses reveals the multifunctional features of their proteins (Sanfacon 2017). Generally, to express the functions of the proteins in virus, interplay of plant proteins with viral proteins is needed (Nagy 2016). Thus, identifying the necessary factors that the hosts need for survival and the host factors that the virus needs for infection and their interactions is the key step in controlling virus disease (Garcia-Ruiz 2018).
During the replication cycle, translation of the viral proteins is necessary for replication, assembly and lastly movement of the virus to the adjacent cells (Garcia-Ruiz 2018). Movement of viruses necessitates plant cellular factors and virus proteins (Wan et al. 2015). For example, with the help of plant cellular factors, MP of plant viruses enables them to enlarge the plasmodesmata path and therefore able to move through cell to cell (Heinlein 2015). This understanding has led to multiple approaches in genetically engineering of plants some of which are produced to remove or deactivate the factors that are necessary for virus infection, importantly without affecting the development of the plants (Pyott et al. 2016).
Genetic plant defense mechanism through RNA interference (RNAi) appears to be an efficient mechanism for counteracting pathogens in many plants (Duan et al. 2012). RNAi is a mechanism where the dsRNA leads to the post-transcriptional gene silencing (PTGS) to inhibit the gene expression (Kim and Rossi 2007). According to Almeida and Allshire (2005), transcription and translation were restrained by corresponding mRNAs which are initiated by dsRNA to silence the target genes. RNAi is also known for the ability to promote resistance towards diseases caused by viruses through virus-induced gene silencing (Ding 2010). Unlike bacteria and fungi, virus multiplies inside the host, which makes the role of RNAi important (Wang et al. 2012). There is direct silencing of the genome of the virus through siRNA that has been demonstrated (Ruize-Ferrer and Voinnet 2009). Bioinformatic research also proposes that miRNAs have the capacity for antiviral mechanism by aiming genomes of virus (Perez-Quintero et al. 2010). Significant examples include the development of transgenic tomato lines constructed with hpRNAi by Mahmoudieh et al. (2019) to induce RNAi pathway and then activate gene silencing. Fuentes et al. (2016) on the other hand showed the resistance of RNAi transgenic tomato plants towards TYLCV.
The precise and early detection of plant pathogens in-field is also critical in light of the rapid changes in the pathogen population due climate change, vector evolution and farm practice (Donoso and Valenzuela 2018). Early detection not only lowers the disease outbreak but also enables farmers to take appropriate control methods rapidly (Pallas et al. 2018). To date, many reviews of available technologies or techniques have been published. Other than the conventional immunological (Martinelli et al. 2014) and morphological techniques (Capote et al. 2012), molecular approaches have been widely utilized, including the use of polymerase chain reaction (PCR)-based techniques such as RT-PCR, real-time PCR, isothermal PCR, ELISA PCR, multiplex PCR and nested PCR (Capote et al. 2012). According to Martinelli et al. (2014), PCR-based techniques provide more advantages than immunoassays based on cost, time and efficiency. PCR-based methods not only faster and cheaper but also manage to detect single target in multiple targets, as well as detect the pathogens that are not able to culture such as bacteria, phytoplasma and viruses (Martinelli et al. 2014). Other technologies include loop-mediated isothermal amplification (LAMP) assay, recombinase polymerase amplification, multiplex immunodetection, microsphere immunoassays (MIA), aptamer-based diagnosis or portable nanopore sequencing; detailed reviews of these can be retrieved from Donoso and Valenzuela (2018). Moreover, Pallas et al. (2018) have also written a review on next-generation sequencing (NGS), multiplex and hybridization technologies for virus detection. Constantly checking for pathogen at its early phase is important as some of the plants will not show symptoms in the early phase; therefore, high-throughput, accurate and highly sensitive technologies are needed (Donoso and Valenzuela 2018).
Conclusion and future perspective
The review of viral diseases in tomato has shown the widespread effects of the diverse pathogens on tomato production in different parts of the world. One reason why viral diseases are of great concern to farmers is because of its diversity and range, fast replication and ease of spread through vectors which enhances its evolution and adaptation towards natural selection pressure (Hanssen et al. 2010). According to Hanssen et al. (2010), the rapid appearance of new viruses could be related to climate change, introduction of new host plants, vectors evolution and cultural practices. The simplicity of its genome is one of the reasons why viruses adapt to the varying environments easily (Jones 2016). The change in climate is thought to be a major causal reason for deteriorating economic production when associated with virus diseases (Pallas et al. 2018). Eastburn et al. (2011) have also reported that the environment plays crucial roles on virus spread and behavior as well as susceptibility of the host. Moreover, climate change also results in alteration of phenology, physiology and morphology of the vectors in addition to affecting host plants (Jones 2016), thus increasing the knowledge on interplays and interactions between pathogen and its antagonist; physiology and ecology of plants and the intermediate vectors are critical for developing strategies for plant protection (Tsitsigiannis et al. 2008). Undeniably, being familiar with the biochemical and molecular structures that consolidate these interplays and interactions is important to unearth effective control methods. On the other hand, the development of simplified and cost-efficient technology has actually facilitated the identification and discovery of the biological properties of the virus and subsequently results in understanding their structure and mechanisms. However, there are still substantive gaps in knowledge as not all of the viruses have been adequately studied due to their large population and high variation among each group, especially under different environmental conditions, stresses, climate and cultural conditions. Studies have shown that through better understanding of these interactions, resistant plant cultivars have been successfully developed in tomato that is resistant to TYLCV, ToTV and ToMarV (Hanssen et al. 2010). For example, introduction of genes controlling resistance to the Begomovirus spp. (Ty genes) from the wild Solanum species (Hanssen et al. 2010). Vidavski et al. (2008) have shown that the Ty resistance genes may interact with each other and results in hybrid plants that have higher resistance than their parental line. The host–virus relationship is governed by a complicated network of interactions. With the increasing availability of genome wide data and big omics data for many of the hosts, pathogens and vectors, the opportunity for elucidating new information on these interactions is growing exponentially. Ultimately the combination of the laboratory research to the application in the field is an approach that should be driven by both researchers and farmers in order to develop sustainable and holistic strategies to limit the spread of virus diseases in this crop.
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Ong, S.N., Taheri, S., Othman, R.Y. et al. Viral disease of tomato crops (Solanum lycopesicum L.): an overview. J Plant Dis Prot 127, 725–739 (2020). https://doi.org/10.1007/s41348-020-00330-0
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DOI: https://doi.org/10.1007/s41348-020-00330-0